Lesions of the dorsal striatum impair orienting behaviour of salamanders without affecting visual processing in the tectum

Eur J Neurosci. 2016 Oct;44(8):2581-2592. doi: 10.1111/ejn.13375. Epub 2016 Sep 5.

Abstract

In amphibians, visual information in the midbrain tectum is relayed via the thalamus to telencephalic centres. Lesions of the dorsal thalamus of the salamander Plethodon shermani result in impairment of orienting behaviour and in modulation of spike pattern of tectal neurons. These effects may be induced by an interruption of a tectum-thalamus-telencephalon-tectum feedback loop enabling spatial attention and selection of visual objects. The striatum is a potential candidate for involvement in this pathway; accordingly, we investigated the effects of lesioning the dorsal striatum. Compared to controls and sham lesioned salamanders, striatum-lesioned animals exhibited a significantly lower number of orienting responses toward one of two competing prey stimuli. Orienting towards stimuli was impaired, while the spike pattern of tectal cells was unaffected, because both in controls and striatum-lesioned salamanders the spike number significantly decreased at presentation of one prey stimulus inside the excitatory receptive field and another one in the surround compared to that at single presentation inside the excitatory receptive field. We conclude that the dorsal striatum contributes to orienting behaviour, but not to an inhibitory feedback signal onto tectal neurons. The brain area engaged in the feedback loop during visual object discrimination and selection has yet to be identified. Information processing in the amphibian striatum includes multisensory integration; the striatum generates behavioural patterns that influence (pre)motor processing in the brainstem. This situation resembles the situation found in rats, in which the dorsolateral striatum is involved in stimulus-response learning regardless of the sensory modality, as well as in habit formation.

Keywords: Plethodon shermani; basal ganglia; midbrain; single-cell recording; telencephalon.

MeSH terms

  • Animals
  • Attention / physiology*
  • Central Nervous System / physiology
  • Neurons / physiology*
  • Orientation / physiology*
  • Photic Stimulation / methods
  • Rats
  • Thalamus / physiology
  • Urodela / physiology*
  • Visual Pathways / physiology*
  • Visual Perception / physiology*